Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved November 21, 2017 (received for review May 26, 2017)
Circumstantial evidence indicates that especially deep-ocean heterotrophic microbes rely on particulate organic matter sinking through the oceanic water column and being solubilized to dissolved organic matter (DOM) prior to utilization rather than on direct uptake of the vast pool of DOM in the deep ocean. Comparative metaproteomics allowed us to elucidate the vertical distribution and abundance of microbially mediated transport processes and thus the uptake of solutes throughout the oceanic water column. Taken together, our data suggest that, while the phylogenetic composition of the microbial community is depth stratified, the composition and substrate specificities of transporters considered in this study are ubiquitous while their relative abundance changes with depth.
The phylogenetic composition of the heterotrophic microbial community is depth stratified in the oceanic water column down to abyssopelagic layers. In the layers below the euphotic zone, it has been suggested that heterotrophic microbes rely largely on solubilized particulate organic matter as a carbon and energy source rather than on dissolved organic matter. To decipher whether changes in the phylogenetic composition with depth are reflected in changes in the bacterial and archaeal transporter proteins, we generated an extensive metaproteomic and metagenomic dataset of microbial communities collected from 100- to 5,000-m depth in the Atlantic Ocean. By identifying which compounds of the organic matter pool are absorbed, transported, and incorporated into microbial cells, intriguing insights into organic matter transformation in the deep ocean emerged. On average, solute transporters accounted for 23% of identified protein sequences in the lower euphotic and ∼39% in the bathypelagic layer, indicating the central role of heterotrophy in the dark ocean. In the bathypelagic layer, substrate affinities of expressed transporters suggest that, in addition to amino acids, peptides and carbohydrates, carboxylic acids and compatible solutes may be essential substrates for the microbial community. Key players with highest expression of solute transporters were Alphaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria, accounting for 40%, 11%, and 10%, respectively, of relative protein abundances. The in situ expression of solute transporters indicates that the heterotrophic prokaryotic community is geared toward the utilization of similar organic compounds throughout the water column, with yet higher abundances of transporters targeting aromatic compounds in the bathypelagic realm.
Author contributions: K.B., O.N.J., and G.J.H. designed research; K.B. and R.R.S. performed research; A.F.-G., R.S., and M.G.P. contributed new reagents/analytic tools; K.B., J.A.L.G., and R.R.S. analyzed data; and K.B., R.S., and G.J.H. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. SRP081826 and SRP081823 (genomic sequence data); KY241481–KY241660, KY194331–KY194691, KY193976–KY194214, KY081807–KY081876, KX426906–KX426937, KX427579–KX428016, KX426472–KX426524, and KX426391–KX426464 (assembled 16S rRNA sequences)]. A selection of Malaspina gene sequences is deposited in Pangaea (https://doi.org/10.1594/PANGAEA.883794).
See Commentary on page 445.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1708779115/-/DCSupplemental.
This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
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